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Journal of Human Evolution 56 (2009) 551–559

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Journal of Human Evolution

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Size and shape variation in the proximal femur of Australopithecus africanus

Elizabeth HarmonDepartment of Anthropology, Hunter College City University of New York, 695 Park Avenue, New York, NY 10065, USA

a r t i c l e i n f o

Article history:Received 12 November 2007Accepted 26 November 2008

Keywords:Intraspecific variationBootstrapCoefficient of variationEuclidean distanceSexual dimorphismHomininHominoidPostcraniaJacovec CavernSterkfonteinMakapansgat

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a b s t r a c t

Aside from use as estimates of body mass dimorphism and fore to hind limb joint size comparisons,postcranial elements have not often contributed to assessments of variation in Australopithecus africanus.Meanwhile, cranial, facial, and dental size variation is interpreted to be high or moderately high. Further,the cranial base and face express patterns of structural (shape) variation, which are interpreted by someas evidence for the presence of multiple species. Here, the proximal femur is used to consider postcranialsize and shape variation in A. africanus. Original fossils from Makapansgat and Sterkfontein, and samplesfrom Homo, Pan, Gorilla, and Pongo were measured. Size variation was assessed by comparing theA. africanus coefficient of variation to bootstrapped distributions of coefficient of variation samplesfor each taxon. Shape variation was assessed from isometrically adjusted shape variables. First, theA. africanus standard deviation of log transformed shape variables was compared to bootstrappeddistributions of logged standard deviations in each taxon. Second, shape variable based Euclideandistances between fossil pairs were compared to pairwise Euclidean distance distributions in eachreference taxon. The degree of size variation in the A. africanus proximal femur is consistent with that ofa single species, and is most comparable to Homo and Pan, lower than A. afarensis, and lower than someestimates of cranial and dental variation. Some, but not all, shape variables show more variation inA. africanus than in extant taxa. The degree of shape difference between some fossils exceeds themajority of pairwise differences in the reference taxa. Proximal femoral shape, but not size, variation isconsistent with high estimates of A. africanus cranial variation.

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Introduction

Australopithecus africanus is known primarily from Member 4 atSterkfontein and Members 3 and 4 at Makapansgat in deposits agedbetween approximately two and three million years (Partridge,1979; Vrba, 1985; Wood, 1985; Partridge and Watt, 1991; Clarke,1994a, 2002; Schwarcz et al., 1994; but see Berger et al., 2002). Thefossil assemblage is partly predator accumulated (Brain, 1981;Pickering et al., 2004) and comprises at least 87 individuals (Pick-ering et al., 2004), mostly represented by craniodental remains. Aunified taxonomy of these remains is generally accepted (Lockwoodand Tobias, 2002), although the pattern of metric and nonmetriccraniodental morphological variation has led to speculation thatmore than one species may be represented (Kimbel and White,1988; Kimbel and Rak, 1993; Clarke, 1994b; Moggi-Cecchi et al.,1998; Partridge et al., 2003). Some metric and nonmetric analysesof the Sterkfontein Member 4 cranial remains do not supporta multiple species interpretation, but indicate a fairly high degree ofsexual dimorphism (Lockwood, 1999; Lockwood and Tobias, 1999).Taken together, craniodental studies suggest that the A. africanushypodigm is characterized by moderate to substantial size and

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shape variation that results from one or more of the followingsampling hypotheses: sexual dimorphism, anagenesis, taphonomicbias, and/or multiple species.

Studies of skeletal size variation among A. africanus postcranialremains indicate a moderate, rather than high, degree of skeletaldimorphism. For example, the distribution of resampled ratios ofA. africanus upper to lower limb joint sizes generated by Green et al.(2007) matches best with the distributions of Homo sapiens and Pantroglodytes, and not highly dimorphic Pongo and Gorilla, implyingmoderate levels of sexual dimorphism. Thus, A. africanus elementsize variation is estimated to be moderate to high, but these esti-mates are generally higher for the cranium than postcranium.

Plavcan (2003) has demonstrated that, in living hominoids,craniofacial dimorphism is paralleled by equal or greater levels ofbody mass dimorphism. The substantial degree of dimorphism of theA. africanus face suggests that body mass dimorphism estimatesderived from postcranial measurements should be high, which is notthe case (McHenry, 1992; Plavcan, 2003). The A. africanus ratio ofapparent male to apparent female body mass is estimated to beclosest to the moderately dimorphic Pan troglodytes (McHenry,1992),which is lower than most estimates of craniofacial dimorphism.

Table 1Extant reference taxa

Taxon n Collection locationa

F M

Homo sapiens40 40 Terry Collection, NMNHAfrican and European Americans

Meroitic period Nubians 8 8 Meroitic Nubian Collection, ASUSouth African Xhosa 20 20 Dart Collection, UW

Gorilla gorilla gorilla 10 11 RCMA; NMNH; MCZGorilla gorilla. graueri 11 11 RMCAPan troglodytes 20 21 RMCA; NMNH; MCZPongo pygmaeus 11 9 NMNH, MCZ; NK

a ASU¼Arizona State University, Tempe; MCZ¼Museum of ComparativeZoology, Cambridge; NK¼Naturkunde, Berlin; NMNH¼National Museum ofNatural History, Washington DC; RMCA¼ Royal Museum for Central Africa, Tervu-ren; UW¼Department of Anatomy, University of Witwatersrand, Johannesburg.

E. Harmon / Journal of Human Evolution 56 (2009) 551–559552

As has been described for the cranial base (e.g., Kimbel andWhite, 1988), there is evidence for substantial non-size relatedmorphological variability among Sterkfontein postcranial remains(Clarke and Tobias, 1995; Partridge et al., 2003). For example, theclavicle from Jacovec Cavern has ape-like conoid tuberclemorphology, while the Member 4 clavicles have more human-likeconoid tubercles (Partridge et al., 2003); although small samplespreclude certainty. Independent of size variation, it is possible thatA. africanus postcrania are characterized by a high degree ofmorphological variation (Clarke and Tobias, 1995; Partridge et al.,2003; Clarke, pers. comm.).

The somewhat different degree of variation (and sexualdimorphism) implied by the postcranial and the craniognathicremains, coupled with the variable morphological pattern in thecranium and among some postcranial elements (e.g., Partridgeet al., 2003; Clarke, pers. comm.), contribute to a lack of under-standing about A. africanus paleobiology. This work aims toexamine skeletal size and shape variation in the proximal femur,one of the best represented postcranial elements. The head of theproximal femur has a relationship to body mass that is understoodfor hominoids (Jungers, 1988; Ruff and Runestad, 1992), stronglysuggesting that the information about size variation in this elementcan be interpreted in a framework that is relatable to estimates ofvariation that are based on body mass (or estimates thereof).

The degree of size and shape variation in the A. africanusproximal femur is identified and described. These results arecompared to the previously documented degree of cranial sizevariation in A. africanus in order to explore the relationshipbetween cranial and postcranial variation in this taxon. Shaperesults are considered in the context of the previously recognizedvariability in cranial and postcranial fossils. Additionally, sizevariation in the proximal femur is compared to that of its congener,A. afarensis.

Methods and materials

Sample and data

Original fossils of eleven adult A. africanus femora with at leastone common measurement are included in this study (MLD 46, Sts14, Stw 25, Stw 99, Stw 311, Stw 392, Stw 403, Stw 479, Stw 501, Stw522, Stw 527) (see SOM). Added to this is the femoral head diam-eter estimate generated from the acetabulum of Stw 431 (McHenryand Berger, 1998: their Table 2) and the femur from the SterkfonteinJacovec Cavern (Stw 598) described by Partridge et al. (2003).Materials from Jacovec Cavern have not been attributed to A. afri-canus, owing to potential morphological differences and to thepresumed earlier date of the Cavern relative to Member 4 (Partridgeet al., 2003; but see Berger et al., 2002). Where noted, the JacovecCavern femur is included in analyses to examine the maximumrange of variation in femora from Sterkfontein.

To establish a context for interpreting size and shape variation inA. afarensis, samples of adult extant hominoid femora of recentHomo, Gorilla, Pan, and Pongo were included (Table 1). A singlespecies or subspecies comprise the sampled genera. Pan femora arefrom two subspecies (Pan troglodytes troglodytes and Pan troglo-dytes schweinfurthii) that are not always separately identified inmuseum collections and are necessarily combined here. Pongofemora are exclusively from Pongo pygmaeus pygmaeus, which issometimes given specific status (Groves, 2001). Gorilla femora arefrom two subspecies, Gorilla gorilla gorilla and Gorilla gorilla graueri.In some taxonomic scenarios (e.g., Groves, 2001) these subspeciescontribute to two distinct species called G. gorilla (which includes G.g. gorilla and G. g. diehli,) and G. beringei (which includes G. g. graueriand G. g. beringei). Here, G. g. gorilla and G. g. graueri are considered

separately and are also combined as G. gorilla. This approachconsiders the presumed minimum degree of variation (subspecies),as well as the combined variation using the traditional taxonomy(G. gorilla). Males and females in each taxon are approximatelyequally represented. Temporal bias in the fossil sample couldpotentially inflate the estimates of variation, but inclusion ofmultiple subspecies in a single reference sample, for example in Pantroglodytes, may mimic the potential effect of this variation (Rich-mond and Jungers, 1995; Lockwood et al., 1996).

While the proximal femoral representation is fairly high inA. africanus, most specimens preserve only the head and neck,which limits the number of measurements that can be taken.Further, the quality of preservation of A. africanus femora is uneven.Many specimens have fossilization cracks or are abraded. Fourmeasurements were taken, including neck height (NH), neckbreadth (NB), head diameter (HD), and morphological neck length(MNL), and are described in Figure 1. Preservation details and fossilmeasurement values can be found in the Online SupplementaryMaterial (SOM; supplementary materials associated with thisarticle can be found in the online version at doi: 10.1016/j.jhevol.2009.01.002).

Analytical methods

A single size variable was established by calculating thegeometric mean of combined measurements (Mosimann, 1970;Jungers et al., 1995). The geometric mean is the nth root of theproduct of n measurements (Sokal and Rohlf, 1995). The coefficientof variation (CV) of geometric means was used to assess size vari-ation in A. africanus and in each of the reference taxa. To accom-modate differential preservation of the fossils and to maximizetheir inclusion, the CV analysis was conducted in three trials basedon the geometric means of five femora for which NH, NB, and HDcould be measured (MLD 46, Stw 99, Stw 311, Stw 501, Stw 522), thegeometric means of eight femora that shared NH and NBmeasurements (MLD 46, Sts 14, Stw 99, Stw 311, Stw 403, Stw 479,Stw 501, Stw 522), and the nine femora with an HD measurement/estimate (MLD 46, Stw 25, Stw 99, Stw 311, Stw 392, Stw 431, Stw501, Stw 522, Stw 527). In addition to being the best representedmeasurement, head diameter was considered alone because therelationship between this linear measurement and body mass isunderstood for apes and humans (Jungers, 1988, 1990), whereas therelationship between each of the other study variables and bodymass is less well understood. The Sterkfontein Jacovec Cavernfemur (Stw 598) was added to each of these trials in a separateanalysis to assess the maximum degree of Sterkfontein andMakapansgat femoral variation.

Fig. 1. Description of measurements.

E. Harmon / Journal of Human Evolution 56 (2009) 551–559 553

Bootstrap resampling was used to generate taxon-specificdistributions of CVs to statistically assess the probability withwhich values equal to, or greater than, A. africanus CV values couldbe sampled in individual extant taxa. The bootstrapping methodentailed randomly obtaining geometric means, with replacement,from reference taxa. For each taxon, 1000 iterations were con-ducted in which the geometric mean of five NH, NB, and MNL; eightNH and NB; or nine HD were retrieved. A CV was calculated andcompiled into distributions of 1000 CVs for each taxon. The samplesize of five, eight, or nine depended on the number of fossil spec-imens that shared the measurements so that the random samplesobtained from hominoid taxa were comparable in size to A. afri-canus (e.g., Lockwood et al., 1996; Arsuaga et al., 1997; Lockwood,1999; Silverman et al., 2001; Harmon, 2006).

Shape was examined in two ways. For both approaches,isometric (but not allometric) size was removed from individualvariables (NH, NB, HD, MNL) by dividing a specimen’s measure-ment by the geometric mean of all its measurements to generateshape variables. In the first approach, the shape variables were logtransformed to ensure correlation of the standard deviation (SD)and mean in the geometrically adjusted data. The SD of logged datawas employed as the measure of relative variation (Lewontin, 1966)and was used to compare variation among taxa. As in the sizeanalysis, the goal was to assess the probability that a value equal to,or greater than, the SD of each A. africanus shape variable could beobtained in the reference taxa. The advantage of this approach wasthat the contribution of each variable to shape variation is acces-sible. The number of femora with each measurement dictated thesize of the random samples obtained from reference taxa. NH, NB,and HD were obtained from six femora (MLD 46, Stw 99, Stw 311,Stw 501, Stw 522, and Stw 598). Morphological neck length wasobtained from four femora (MLD 46, Stw 99, Stw 522, and Stw 598).As in the size analysis, 1000 iterations were conducted for eachshape variable in each taxon wherein the means and SD of a sample,sized 4 or 6, were calculated from log transformed size adjusteddata. Taxon-specific distributions of these results were used asa basis of comparison to A. africanus shape variation as indicated bythe SD.

Shape was also examined using the Euclidean distance (ED)between combinations of shape variables. An ED matrix of pair-wise comparisons of the shape variables was generated for fossilpairs that had preserved NH, NB, MNL, and HD, and again for fossilpairs that had preserved NH, NB, and HD, resulting in two sets ofcombined measurements. Euclidean distances derived from eachof the two sets of combined measurements provided a gauge ofthe phenetic affinity of fossil pairs, with smaller values indicatinggreater similarity than larger values (Lague and Jungers, 1996). Inorder to interpret the fossil ED magnitudes, EDs based on each ofthe two sets of measurements were calculated for all possiblepairs in each reference species (Lague and Jungers, 1996). For each

taxon and the two sets of combined measurements, the propor-tion of distance values equal to, or greater than, those of fossilpairs was determined. Unlike the CV size and log SD shape anal-ysis in which the probability of a value as great or greater thanthat of A. africanus could be obtained, the ED analysis conveyedonly the proportion of values as great or greater than those ofA. africanus, which could not easily be interpreted in terms ofstatistical significance.

Results

Analysis of size variation

Table 2 presents descriptive statistics for size by taxon and byindividual measurement. The A. africanus NH, NB, and HD CV is 11.2,the NH and NB CV is 11.4, and the HD CV is 7.7 (Table 2). With theinclusion of the Jacovec Cavern femur (Stw 598), the CV values arereduced to 10.9, 10.5, and 7.5, respectively (Table 2). The taxon NH,NB, and HD CV magnitude is greatest in Gorilla, followed by Pongo,A. africanus, H. sapiens, and is smallest in Pan (Table 2). The patternis the same for the CV based on NH and NB, as well as that based onHD (Table 2).

The results of the bootstrap analysis are tabulated in Table 3, andthe results for the combined CVs are displayed in Figure 2. Theprobability of sampling CV values as great, or greater than, that of A.africanus is higher than 5% in each taxon for each variable set.Therefore, based on size variation in proximal femoral variables,a single species hypothesis cannot be rejected for A. africanus.

In the bootstrap analysis, between 9% and 83% of NH, NB, and HDCVs in extant taxa equal or exceed that of A. africanus. Only 9% and10% of Pan troglodytes and H. sapiens respectively equal or exceedthe A. africanus value of 11.2. The more sexually dimorphic taxaequal or exceed the A. africanus value in substantially higherpercentages, such as 71% for Pongo. For NH and NB, the probabilityof sampling a value as great as or greater than that of A. africanusranges from low in Homo (5%) to very high in G. g. gorilla (97%). Theprobability of sampling 11.4 or greater in Pan troglodytes is fairlylow (14%), but is higher in Pongo (77%) and G. g. graueri (83%).Nearly all random samples of Gorilla and Pongo resulted in equal orhigher HD CV values than that of A. africanus. In comparison, only17% of Pan and 34% of Homo sample CVs were equal to or greaterthan 7.7. Size variation in A. africanus femora is within the range ofextant taxa and appears to be less than that of the strongly sexuallydimorphic apes, but slightly greater than that of humans andchimpanzees.

Analysis of shape variation

Unlike size variation, which is within the range of single species,the degree of shape variation is sometimes outside the range of

Table 2Descriptive statistics by taxon for individual and combined measurements

MNL NH NB HD NH, NB, HD NH, NB

A. africanus (# fossils) Mean 38.9 (3) 24.1 (9) 16.9 (8) 34.0 (9) 24.6 (5) 20.3 (8)SD 9.1 2.5 2.1 2.6 2.3 2.1CV 23.4/19.0a 13.2/12.6a 12.6/12.2a 7.7/7.5a 11.2/10.5a 11.4/10.8a

G. gorilla Mean 36.3 32.7 26.2 47.2 35.4 29.4SD 5.3 4.8 4.6 6.5 5.3 4.7CV 14.6 14.8 17.5 13.8 15.0 16.0

G. g. gorilla Mean 37.2 32.1 26.1 46.5 34.9 29.1SD 6.0 5.2 5.1 6.3 5.5 5.1CV 16.2 16.3 19.4 13.6 16.0 17.5

G. g. graueri Mean 35.4 33.3 26.3 48.0 35.9 29.8SD 4.3 4.4 4.2 6.9 5.2 4.3CV 12.2 13.3 15.9 14.3 14.2 14.3

H. sapiens Mean 33.2 30.7 25.8 44.1 33.5 28.2SD 4.6 3.6 3.1 3.8 3.5 3.3CV 14.0 11.6 12.0 8.6 9.9 11.2

Pan troglodytes Mean 24.8 22.1 18.7 32.9 14.7 20.4SD 3.8 2.1 1.9 2.2 2.1 2.0CV 15.5 9.4 10.1 6.7 8.2 9.5

Pongo pygmaeus Mean 26.2 21.2 16.6 34.2 22.9 18.7SD 3.9 2.8 2.5 4.3 3.0 2.6CV 14.9 13.4 15.3 12.7 13.2 13.9

a CV calculated with Stw 598 (Jacovec femur).

E. Harmon / Journal of Human Evolution 56 (2009) 551–559554

single taxa. Table 4 demonstrates that it is not possible to samplethe A. africanus SD of mean, log, and size adjusted NB and NH in G. g.graueri, Pan troglodytes, or H. sapiens. The probability of samplinga SD of mean, log, and size adjusted HD as great, or greater than,that of A. africanus is between 19% and 24% in Pongo pygmaeus, G. g.gorilla, and Pan troglodytes, but is zero in G. g. graueri and H. sapiens.On the other hand, the log SD of MNL is regularly sampled in eachtaxon (12% or higher). These analyses include the Jacovec Cavernfemur (Stw 598), because there is no indication that its inclusionsubstantially increases size variation (see above). However, Stw 598was informally removed in SD shape analysis to determine whetherestimates of variation were reduced, the values remainedunchanged, or were slightly increased.

The pairwise Euclidean distances based on shape ratios helpdiscern how individual fossils contribute to shape variation andprovide information about phenetic affinity among fossils. Thereare four fossils for which the four shape variables could be included(MLD 46, Stw 99, Stw 522, Stw 598). Euclidean distance values forpairwise comparisons among these four femora are presented inTable 5. The ED values for the pairs Stw 99 and Stw 522 (0.35) andStw 99 and MLD 46 (0.41) are much larger than for other fossilpairs. The probability of sampling an ED value as great as thoseassociated with the Stw 99 pairs mentioned above is less than fivepercent in all taxa except Pongo pygmaeus (for Stw 99 vs. Stw 522).On the other hand, the ED value between Stw 99 and Stw 598 (0.15)is the smallest among the fossil pairs and is equal to or smaller thanover one third of individual taxon ED values. Pairwise comparisonsbetween Stw 522 and MLD 46, and between Stw 522 and Stw 598result in EDs that are comparable to, or smaller than, at least 14% ofthose in extant taxa. The pairing of MLD 46 and Stw 598 is matchedor exceeded by only 6% to 10% of Gorilla pairs, 10% of Homo pairs,11% of Pan pairs, but 21% of Pongo pairs.

Shape variables NH, NB, and HD could be generated for sixfemora (MLD 46, Stw 99, Stw 311, Stw 501, Stw 522, Stw 598). The

Table 3Probabilities of sampling CVs in extant hominoid samples equal to or greater than those

Measurements G. gorilla G. g. graueri G. g. goril

NH, NB, HD (11.2) 0.80 0.76 0.83NH, NB (11.4) 0.92 0.83 0.97HD (7.7) 0.98 0.99 0.98

pairwise ED values appear in Table 6. Pairs that include Stw 501 orMLD 46 result in EDs that are commonly accommodated in extanttaxa (except when MLD 46 is paired with Stw 522, see Table 6).Pairs that include Stw 311 result in EDs that are accommodated inextant taxa in low proportions. The proportions are particularly lowwhen Stw 311 is paired with Stw 99 and Stw 598. The ED valuesresulting from these pairings are matched or exceeded by 1% or lessof G. g. graueri pairs, and no more than 19% of other extant pairs. TheStw 99 and Stw 598 pairwise value is the smallest of all the pairsthat include Stw 99 (0.06) and is most often matched or exceeded inextant taxa. On the other hand, the large ED between Stw 99 andStw 522 (0.20) is greater than over 95% of pairs in each extanttaxon. The ED between Stw 598 and Stw 522 (0.15) is equal to orlarger than all G. g. graueri pairs and at least 87% of the pairs in othertaxa. Except when paired with Stw 311 or Stw 522, EDs associatedwith Stw 598 (Jacovec femur) are low and are easily accommodatedin extant taxa. The smallest ED value among the fossil pairs isbetween MLD 46 and both Stw 501 and Stw 598 (0.04) and thelargest is between Stw 99 and Stw 522 (0.20).

Shape variation is moderate to high among A. africanus proximalfemora. Sources of elevated variation include the variables NH, NB,and to a lesser extent, HD. Femora associated with elevated varia-tion when three variables are considered include Stw 99, Stw 311,Stw 522, and Stw 598. When four variables are used, all femora(Stw 99, Stw 522, Stw 598, and MLD 46) contribute to high EDs insome pairings.

Discussion

Size variation

The CV results suggest that A. africanus hind limb size variationis comfortably within the range of the examined hominoid taxa.The inclusion of Stw 598 does not increase CV estimates. Therefore,

obtained for Australopithecus africanus

la Pongo pygmaeus Pan troglodytes H. sapiens

0.71 0.09 0.100.77 0.14 0.050.99 0.17 0.34

Fig. 2. Resampled CV distributions by taxon for NH, NB, HD, and NH and NB with A. africanus values indicated by single black line.

E. Harmon / Journal of Human Evolution 56 (2009) 551–559 555

the degree of proximal femoral size variation provides no directevidence for the presence of multiple species in A. africanus, evenwith the inclusion of the Jacovec Cavern femur. The likelihood ofsampling A. africanus levels of size variation using three variablesand five fossils, or two variables and eight fossils is lowest inH. sapiens and Pan troglodytes, whereas, resampled CVs obtainedfrom highly sexually dimorphic Pongo and Gorilla were greater

than those of A. africanus the majority of the time. The coefficientof variation in a sample has been shown to be strongly correlatedwith sexual dimorphism in the sample (Plavcan, 1994; Ko�scinskiand Pietraszewski, 2004). Thus, the degree of skeletal dimorphismimplied by these findings places A. africanus somewhere close toPan troglodytes and lower than Pongo pygmaeus. This level ofskeletal dimorphism is slightly less than the body mass

Table 4Probability of sampling shape variable SD in extant hominoids equal to, or greater than, Australopithecus africanus

Shape variable A. africanusLog Mean/SD

G. g. graueri G. g. gorilla G. gorilla Pongo pygmaeus Pan troglodytes H. sapiens

NH 0.02/0.03 0.00* 0.26 0.12 0.18 0.00* 0.02*HD 0.14/0.02 0.00* 0.24 0.08 0.19 0.23 0.00*NB 0.14/0.03 0.00* 0.11 0.07 0.13 0.01* 0.01*MNL 0.15/0.05 0.24 0.25 0.26 0.55 0.38 0.12

* Probabilities that are less than 0.05.

E. Harmon / Journal of Human Evolution 56 (2009) 551–559556

dimorphism estimate of McHenry (1992), which placed A. africanusbody mass dimorphism between Pan and Gorilla (Pongo was notincluded).

The CV results in Tables 2 and 3 illustrate a difference betweenskeletal dimorphism and body mass dimorphism. The taxon (notresampled) CV values in Table 2 are generally higher in recenthumans than in chimpanzees, implying that the former is moresexually dimorphic than the latter. This is a skeletal phenomenon,actual body mass dimorphism is demonstrably greater in Pan thanin humans (McHenry, 1992; Smith and Jungers, 1997; Lague, 2003;Plavcan et al., 2005). Further, the high degree of femoral headvariation in recent humans results in body mass dimorphismestimates from femoral head size that are inflated (e.g., Plavcanet al., 2005: 316–317), while body mass dimorphism estimates fromgreat ape femoral heads are not inflated (e.g., Jungers, 1988; Ruffand Runestad, 1992).

In Table 3, the probability of sampling an HD value as great, orgreater than, that of A. africanus is substantially higher than theprobability of sampling the NH and NB CV estimate in H. sapiens(34% for HD and 5% for NH and NB). The probability of sampling anHD value as great, or greater than, that of A. africanus in Pan trog-lodytes is lower than in H. sapiens (34% in Homo and 17% in Pan), andis similar to the Pan troglodytes NH and NB probability (17% for HDand 14% for NH and NB). In fact, within each ape taxon all three CVprobabilities imply a consistent degree of variation in relation tothat of A. africanus, while this is not the case for Homo, whichimplies a different degree of variation in relation to A. africanusbased on HD CV compared to NH and NB CV (see Table 3). This is aninteresting result that may indicate that the pattern of size varia-tion in A. africanus proximal femora is not like the pattern of sizevariation in humans. That is, the relationship among CV estimatesin A. africanus is most consistent with the relationship among CVestimates in great apes, and not with the relationship among CVestimates in humans, which reflect a large difference between HDand non-HD CV probabilities not present in other taxa. Althoughspeculative, this may signal a great ape relationship, rather thanhuman relationship, between femoral head diameter and bodymass dimorphism for A. africanus.

Inspection of Figure. 2 shows the A. africanus CV for combinedmeasurements falling well inside the distributions of Homo and PanCVs. This information, combined with the cumulative A. africanusCV and individual measurement CVs in Table 2 places variation near

Table 5Shape variables NH, NB, HD, MNL. Proportion of pairwise Euclidean distance value as gr

Fossil comparison ED value G. gorilla G. g. gorilla

Stw 99 and Stw 522 0.35 0.01 0.01Stw 99 and MLD 46 0.41 0.00 0.00Stw 99 and Stw 598 0.15 0.45 0.51Stw 522 and MLD 46 0.18 0.33 0.36Stw 522 and Stw 598 0.22 0.19 0.22MLD 46 and Stw 598 0.27 0.09 0.10

that of Pan, and near or slightly above that of Homo. Therefore, theproximal femoral level of size variation is moderate and is slightlylower than facial variation. When assessed by similar resamplingmethods, facial variation was interpreted to be between Pan andGorilla when (Lockwood, 1999). Proximal femoral size variation islower than reported molar size variation where the distribution ofvariation in A. africanus molar breadths is nearly bimodal (Kimbeland White, 1988).

It is surprising to find skeletal size variation that is less thancraniofacial size variation. In hominoids, substantial cranial varia-tion and size dimorphism is matched or exceeded by body massdimorphism (Plavcan, 2003). These results, which approximate(but do not directly assess) skeletal dimorphism cannot be easilycompared to body mass dimorphism. It is possible that A. africanusskeletal dimorphism is lower than body mass dimorphism,meaning that actual A. africanus body mass dimorphism is notlower than craniofacial dimorphism. On the other hand, some(Lockwood, 1999; Plavcan, 2003) have suggested that, in departurefrom extant hominoids, a pattern of higher levels of craniofacialcompared to body mass dimorphism may characterize early hom-inins. However, it is important to note that A. afarensis appears toexpress similar postcranial and cranial levels of skeletal variation bymost accounts (McHenry, 1986; Kimbel and White, 1988; McHenry,1992; Lague and Jungers, 1996; Lockwood et al., 1996; Lockwoodet al., 2000; Lague, 2003; Plavcan et al., 2005; Harmon, 2006; butsee Reno et al., 2003, 2005 for an alternate view of postcranialvariation).

Like A. africanus, size variation among A. afarensis proximalfemora is also within the range of extant taxa (Harmon, 2006).However, the degree of femoral size variation in A. africanus ismarkedly lower than that of A. afarensis, assuming that the samplesused to assess variation adequately represent taxon variation andnot sampling bias (see below). Under a single species model, thedegree of variation and, by extension, sexual dimorphism in the A.afarensis femoral sample is greater than in Pongo but less than inGorilla (Harmon, 2006, but see Reno et al., 2003 for an interpreta-tion of lesser postcranial variation in A. afarensis). Here, based onsimilar methods, the degree of A. africanus sexual dimorphismunder a single species model is found to be like that of Pan andlower than that of Pongo. Likewise, Green et al. (2007) found thedegree of size variation in A. africanus limb size proportions to belower than that of A. afarensis.

eat or greater than Australopithecus africanus

G. g. graueri Pongo pygmaeus Pan troglodytes H. sapiens

0.01 0.09 0.04 0.040.02 0.04 0.01 0.020.37 0.56 0.50 0.470.26 0.45 0.36 0.330.14 0.34 0.22 0.200.06 0.21 0.11 0.10

Table 6Shape variables NH, NB, HD. Proportion of pairwise Euclidean distance value as great or greater than Australopithecus africanus

Fossil comparison ED value G. gorilla G. g. gorilla G. g. graueri Pongo pygmaeus Pan troglodytes H. sapiens

Stw 501 and Stw 311 0.08 0.46 0.44 0.34 0.44 0.40 0.50Stw 501 and Stw 99 0.12 0.19 0.24 0.07 0.25 0.19 0.22Stw 501 and Stw 522 0.08 0.46 0.44 0.34 0.44 0.40 0.50Stw 501 and MLD 46 0.04 0.80 0.69 0.70 0.73 0.75 0.82Stw 501 and Stw 598 0.08 0.46 0.44 0.34 0.44 0.40 0.50Stw 311 and Stw 99 0.15 0.07 0.12 0.00 0.13 0.10 0.10Stw 311 and Stw 522 0.11 0.25 0.29 0.12 0.27 0.23 0.27Stw 311 and MLD 46 0.10 0.30 0.36 0.18 0.31 0.27 0.33Stw 311 and Stw 598 0.14 0.10 0.15 0.01 0.19 0.13 0.13Stw 99 and Stw 522 0.20 0.01 0.03 0.00 0.03 0.02 0.03Stw 99 and MLD 46 0.08 0.45 0.48 0.32 0.43 0.39 0.49Stw 99 and Stw 598 0.06 0.64 0.58 0.53 0.59 0.57 0.67Stw 522 and MLD 46 0.12 0.18 0.22 0.05 0.25 0.18 0.21Stw 522 and Stw 598 0.15 0.07 0.12 0.00 0.13 0.10 0.10MLD 46 and Stw 598 0.04 0.80 0.69 0.70 0.73 0.75 0.82

E. Harmon / Journal of Human Evolution 56 (2009) 551–559 557

Shape variation

Femoral shape variation appears to be greater than femoral sizevariation. That is, while size variation in A. africanus is never greaterthan size variation in extant taxa, shape variation is greater than inextant taxa in some assessments. Variation in the A. africanus shapevariable MNL is comparable to other taxa, but variation in the NHand NB shape variables is high compared to all taxa, and cannot besampled in G. g. graueri, Pan troglodytes, and H. sapiens. Variation inthe A. africanus HD shape variable is outside the range of Homo andG. g. graueri. These results allow identification of NB and NH as themajor contributors to shape variation in A. africanus, followed byHD.

Some shape variable pairwise comparisons among fossils resultin EDs that are greater than those in extant taxa, while others resultin EDs that are the same or smaller than those in extant taxa. Thefemur that consistently contributes to the highest EDs is Stw 99.Stw 99 shares greatest affinity with Stw 598, and is least like MLD46 (when four variables are considered) and Stw 522 (when threeare considered). The Jacovec femur (Stw 598), which is not formallyattributed to A. africanus, compares closely in shape with MLD 46and Stw 99 when all shape variables are considered and only Stw99 when fewer variables are considered. The close affinity of Stw 99and Stw 598 agrees with the observation of Partridge et al. (2003)that the two femora share a long neck. The ED between Stw 598and Stw 522 is greater than between Stw 598 and Stw 99, which isalso consistent with Partridge et al. (2003), who noted the shorterneck of Stw 522 compared to Stw 598. When MNL is removed, Stw99, MLD 46, and Stw 501 are most like Stw 598, while Stw 311 andStw 522 are least like Stw 598. Thus, Stw 99 is least like other fossilswhen the MNL shape variable is included. Additionally, Stw 598contributes to large ED values in all variable combinations. Thesefindings help to identify Stw 99 and possibly, Stw 598 (from JacovecCavern), as fossils that might be responsible for inflating shapevariation estimates.

The degree of A. africanus proximal femoral shape variation ishigher than that of A. afarensis (Harmon, 2006). In the latter case,fewer femora contributed to shape analysis, but only one (A.L. 128-1) was somewhat different from the others. Proximal femoral shapevariation is also high compared to extant taxa, but it is difficult tounequivocally state that it is too high to be accommodated ina single species. For example, variation in the NH and NB shapevariables is outside the range of some, but not all extant taxa, whilevariation in the shape variable MNL is not outside the range of anyextant taxon.

Shape variation in the proximal femur of A. africanus is greaterthan size variation in this element. Further, size variation in A.africanus is lower, and shape variation is higher, than in A. afarensis.

This result is surprising given the general morphological similaritybetween these two taxa, such as the long and narrow femoral necksthat characterize both species (Harmon, 2005, 2009; Richmond andJungers, 2008).

Potential limitations and possible explanations

As is often the case with fossil material, some femora are in lessthan ideal condition (see SOM) and poor preservation may haveinfluenced the results. The preservation of Stw 99 in particular mayinfluence the obtained measurements. For example, while Stw 99exhibits an obviously long femoral neck, the surface of the fossil issomewhat abraded. Because the external surface of the head isvirtually absent, HD is underestimated, although Stw 99 does nothave the smallest HD value. An underestimate might affect shapevariation results because HD is a shape variable and contributes tothe geometric mean that underlies other shape variables. Never-theless, Stw 99 is phenetically very similar in pairwise analyses toStw 598, which has no preservation issues (see Partridge et al.,2003). The similarity between the two fossils confirms visual andmetric assessments that Stw 99 and Stw 598 do indeed sharea longer neck in combination with a somewhat smaller head thanother A. africanus femora.

Other preservation irregularities are seen in MLD 46, which suffersfrom fossilization cracks and surface erosion; Stw 501 has an erodedsurface and Stw 527 is cracked, which may influence their headdiameter estimates. MLD 46 has the largest femoral head in the A.africanus group, which could be an artifact of cracks rather thana reflection of true morphology. If so, variation in head shape might beinflated, although it should be reflected in HD CV estimates, which itdoes not appear to be. Because of incomplete preservation, it wasimpossible to measure NH and NB of Stw 392 and Stw 479 at themidpoint of the neck as was done with most fossils. This may meanthat these measurements are not comparable to the others. The HDestimate of Stw 431 was based on the acetabulum because the headitself is not preserved (McHenry and Berger, 1998). It is difficult todetermine precisely how these preservation issues influence studyoutcomes. Cracked, and thus, expanded surfaces likely lead to over-estimated values. On the other hand, surface abrasion leads tounderestimated values. Given that both problems affect the sample,sometimes in a single specimen (e.g., MLD 46), the overall influenceon variation may be random, although directional influences may beidentifiable for a few specific fossils (e.g., Stw 99).

Sampling error, another common problem in fossil studies,could influence the current results. For example, the CV is a betterestimator of sample variation when sample sizes equal 20 thanwhen sample sizes equal five (Cope and Lacy, 1995). Although theCV was not used to calculate sexual dimorphism in the manner of

E. Harmon / Journal of Human Evolution 56 (2009) 551–559558

Plavcan (1994) and Ko�scinski and Pietraszewski (2004), it is likelythat the same sampling biases that influenced their results(unbalanced sex ratio, small samples, and high intrasexual varia-tion) may influence estimates of variation found here. Additionally,it is possible that as a result of predator selection (Brain, 1981;Pickering et al., 2004), size variation in postcranial elements isconstrained. If a predator bias exists, size variation found here inthe Makapansgat and Sterkfontein may be under (or over)estimated.

While preservation and sampling issues are important toconsider, other explanations for the current results are worthproposing. It might be that femoral shape variation results aretracking an evolving lineage that changed in shape, but not in size.Alternatively, allometric effects or time averaging could result ininflated shape variation estimates, although temporal effects in theA. afarensis cranium, for example, were recognized in size variation,not shape variation (Lockwood et al., 2000). If present, size-relatedshape variation not accounted for in isometric adjustment couldinflate shape variation. Another possibility is that two species,which differ in shape but not necessarily is skeletal size are in factpresent in the A. africanus femoral sample.

Conclusions

Size variation in the proximal femur of A. africanus is well withinthe range of that of extant taxa. This result holds when the fullcomplement of published Makapansgat and Sterkfontein femora isconsidered, including Stw 598 from the potentially youngerdeposits of Jacovec Cavern (Partridge et al., 2003). This studyprovides no direct evidence for the presence of multiple species onthe basis of size. However, the possibility exists that multiplespecies are present that cannot be detected in femoral size varia-tion. In fact, some variation in the cranial base and face is not size-related, but relates to shape differences that are interpreted aseither excessive for a single taxon by some, or great but notinconsistent with a single species by others (Clarke, 1988; Kimbeland White, 1988; Kimbel and Rak, 1993; Ahern, 1998; Lockwood,1999). The degree of sexual dimorphism implied by size variation isbetween that of humans/chimpanzees and orangutans, anddistinctly lower than that of A. afarensis. To the extent that skeletaldimorphism reflects body mass dimorphism (and it may not),lower levels of dimorphism in the body compared to the face of A.africanus is obtained. This is a departure from the extant hominoidscaling pattern identified by Plavcan (2003).

Previous descriptions of morphological variation in the craniumand postcranium suggest that shape variation in the A. africanusproximal femur is likely to be high (Clarke and Tobias, 1995;Partridge et al., 2003). On the basis of shape but not size, thisappears to hold true. For example, Stw 99 differs from many of theother femora, but is similar to the Jacovec Cavern femur. Further,shape (but not size) variation of neck variables is higher than inreference taxa. Small samples and a low level of statistical power inshape analyses (for example ED pairwise analysis) prohibit firmconclusions about the taxonomic meaning of high shape variationin A. africanus proximal femora.

Potential sampling bias and less than ideal fossil preservationmay have influenced the current results. Therefore, other post-cranial elements must be examined in order to clarify the natureand degree of shape variation in A. africanus postcrania, the rela-tionship of skeletal size variation to craniofacial variation, and thedifferences in pattern of variation between A. africanus and A.afarensis. The parsimonious assumption based on this analysis ofsize and shape is that the proximal femoral sample, which is thelargest among A. africanus postcranial elements, represents a singlespecies that exhibits a moderate to high degree of shape variation,

and a moderate degree of size variation that is somewhere betweenthat of orangutans and chimpanzees.

Acknowledgements

The author thanks Francis Thackeray and Kevin Kuykendall forassistance and access to fossil material. Several others providedaccess to comparative collections, including Diane Hawkey, WimVan Neer, Judy Chupasko, Linda Gordon, David Hunt, and RobertAsher. Ron Clarke generously discussed the Sterkfontein fossils.Conversations about analytical methods with the late CharlieLockwood were invaluable for successful completion of this work,and his wise counsel will be missed. The comments of the anony-mous reviewers, the Associate Editor, and Susan Anton wereextremely helpful in finalizing this manuscript. This work wassupported by NSF BCS 0333296 and the American Association ofUniversity Women.

Appendix. Supplementary data

Supplementary data associated with this article can be found inthe online version, at doi: 10.1016/j.jhevol.2009.01.002

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